Scurvy in the Year 2000

An Orange a Day Keeps the Doctor Away: Scurvy in the Year 2000

Michael Weinstein, MD*; Paul Babyn, MD‡; and Stan Zlotkin, MD*

ABSTRACT. Scurvy has been known since ancient Her past medical history was remarkable for moderate global times, but the discovery of the link between the dietary developmental delay, mild facial dysmorphism, and a seizure deficiency of ascorbic acid and scurvy has dramatically disorder managed with long-term phenytoin administration. She reduced its incidence over the past half-century. Sporadic had 2 older sisters with a similar disorder, and a previous evaluation had not identified a known, inherited condition. reports of scurvy still occur, primarily in elderly, isolated She was admitted to a community hospital with a 2-month individuals with alcoholism. The incidence of scurvy in history of increasing bilateral knee pain and swollen, bleeding the pediatric population is very uncommon, and it is gums. There was no history of fever, weight loss, trauma, obvi- usually seen in children with severely restricted diets ously swollen joints, petechiae, or bruising. At the time of her attributable to psychiatric or developmental problems. hospitalization, the child refused to walk. She previously ambu- The condition is characterized by perifollicular petechiae lated with the aid of a walker. and bruising, gingival inflammation and bleeding, and, Investigations at that time revealed a hemoglobin of 79 g/L, ϫ 9 in children, bone disease. We describe a case of scurvy in white blood cell count of 8.9 10 /L with a normal differential ϫ 9 a 9-year-old developmentally delayed girl who had a diet count and a platelet count of 470 10 /L. A blood smear showed markedly deficient in vitamin C resulting from ex- hypochromic, microcytic red blood cells; no malignant cells were seen. The erythrocyte sedimentation rate was elevated at 62 mm/ tremely limited food preferences. She presented with hour. The C-reactive protein level was 125 mg/L (reference range: debilitating bone pain, inflammatory gingival disease, 0–8 mg/L). Radiographs of the knee showed osteopenia, and a perifollicular hyperkeratosis, and purpura. Severe hyper- bone scan initially showed increased uptake around the left knee. tension without another apparent secondary cause was She was treated presumptively for osteomyelitis with intravenous also present, which has been previously undescribed. clindamycin, but after 2 weeks of therapy, there was no improve- The signs of scurvy and hypertension resolved after ment, and a repeat bone scan was interpreted as normal. Addi- treatment with vitamin C. The diagnosis of scurvy is tional studies included a negative antinuclear and rheumatoid made on clinical and radiographic grounds, and may be factor, and normal complement, creatine kinase, calcium, phos- supported by finding reduced levels of vitamin C in phate, alkaline phosphatase, and parathyroid hormone levels. She required regular ibuprofen and codeine for analgesia. Because of serum or buffy-coat leukocytes. The response to vitamin her gingival disease, which was felt to possibly be secondary to C is dramatic. Clinicians should be aware of this poten- phenytoin, she underwent a gingivoplasty and dental extractions. tially fatal but easily curable condition that is still occa- The biopsy showed chronic inflammatory cells in the submucosa sionally encountered among children. Pediatrics 2001; without evidence of malignancy. Although in hospital, hyperten- 108(3). URL: http://www.pediatrics.org/cgi/content/full/ sion was noted with blood pressure measurements ranging from 108/3/e55; scurvy, hypertension, magnetic resonance 130 to 170/80 to 110 mm Hg. She was transferred to a tertiary care imaging, bone pain. institution for additional evaluation. On physical examination, weight and height were between the 10th and 25th percentiles for age. Her blood pressure was 160/110 ABBREVIATION. MRI, magnetic resonance imaging. mm Hg. She had mild, dysmorphic features with epicanthic folds, mid-face hypoplasia, broad nasal tip and short, broadened hands. She had markedly swollen, purple, spongy gingiva which bled 9-year-old girl with global developmental spontaneously (Fig 1). Her cardiovascular examination was nor- delay presented with signs of scurvy second- mal with no blood pressure gradient between her upper and lower extremities. There was no hepatosplenomegaly or lymphadenop- Aary to long-term ascorbic acid deficiency and athy. Musculoskeletal examination showed soft-tissue swelling of was also discovered to have severe hypertension. the distal wrists and left suprapatellar area. She had decreased This case highlights a rare disease that still exists in range of motion of her knees bilaterally with a fixed flexion the pediatric population and points to a possible contracture of 30° at the left knee. There were no joint effusions. Her skin showed follicular hyperkeratosis with perifollicular pur- association between hypertension and vitamin C de- pura of the lower extremities. Neurologic examination was nor- ficiency. Magnetic resonance imaging (MRI) findings mal. of scurvy, which have been previously unreported, A skeletal survey revealed generalized osteopenia, evidence of are described. T7-T10 vertebral compression fractures, and dense lines at the distal left femoral metaphysis. The findings were not felt to be CASE REPORT indicative of rickets, scurvy, or a storage disorder. A bone scan showed increased uptake only at sites corresponding to the ver- A 9-year-old girl was admitted to hospital because of muscu- tebral compression fractures. An MRI study showed a diffuse, loskeletal pain, inflammatory gingival disease, and hypertension. symmetrically abnormal signal involving the distal femoral metaphyses and epiphyses, both iliac bones, distal radii, and soft tissue surrounding the knees (Fig 2). From the Departments of *Paediatrics and ‡Radiology, Hospital for Sick Initial concern was whether a malignant process was responsi- Children and University of Toronto, Toronto, Canada. ble for her presentation. A bone marrow aspirate and biopsy Received for publication Mar 8, 2001; accepted May 8, 2001. showed no evidence of malignancy or storage cells. There were no Address correspondence to Michael Weinstein, MD, Hospital for Sick Chil- stainable iron stores. Biopsy of the distal femoral metaphysis dren, Department of Paediatrics, 555 University Ave, Toronto, Canada M5G showed nonspecific fibrous changes with no evidence of malig- 1X8. E-mail: [email protected] nancy. The constellation of bone and gingival disease, follicular PEDIATRICS (ISSN 0031 4005). Copyright © 2001 by the American Acad- hyperkeratosis, and perifollicular purpura strongly suggested a emy of Pediatrics. diagnosis of scurvy. The patient’s diet consisted of water, com- http://www.pediatrics.org/cgi/content/full/108/3/Downloaded from www.aappublications.org/newse55 by PEDIATRICS guest on September Vol. 25, 108 2021 No. 3 September 2001 1of5 Fig 1. Photograph demonstrating marked gingival hypertrophy, swelling, and bleeding.

TABLE 1. Selected Nutritive Value of Patient’s Diet* and Rec- ommended Intake Vitamin C Vitamin D Iron 2% Milk (1 cup) 2 mg 2.3 ␮g 0.12 mg Commercial chocolate 0 mg Unknown 0.72 mg puddings (3.5 oz) Heinz pureed meat (100 mL) 2 mg Unknown 1.63 mg Daily recommended nutrient 25 mg 5.5 ␮g8mg intake for age† * Source: Bowes and Church’s Food Values of Portions Commonly Used. 15th ed. New York, NY: Harper & Row; 1989. † Source: Standing Committee on the Scientific Evaluation of Dietary Reference Intakes. Food and Nutrition Board. Institute of Medicine. Washington, DC: National Academy Press; 2000

24-hour urine vanillylmandelic acid and homovanillic acid levels. Her electrocardiogram and echocardiogram showed borderline left ventricular hypertrophy. The child and family were assessed by the clinical genetics and metabolics services. The skeletal survey was not felt to be suggestive of a lysosomal storage disease. Investigations including a karyotype on peripheral blood, urine for oligosaccharides, muco- polysaccharides, and organic acids, leukocyte assays for ␤-galac- Fig 2. Coronal T1-weighted MRI image of the thighs demonstrat- tosidase and hexosaminidase, and blood for quantitative amino ing high signal within the bone and adjacent musculature (arrow). acids, lactate, and ammonium were normal. A skin biopsy was performed for additional fibroblast cultures. No diagnosis of the underlying condition affecting the child and her siblings was mercial chocolate puddings and cakes, occasional jarred semipu- established, and the family continues to be followed by the genet- reed foods (beef, spaghetti), and 2% milk (8 oz/d). She took no ics service. vitamin supplements. By her family’s recollection, she had not Treatment was started with 250 mg of vitamin C, 800 U of consumed fresh fruits or vegetables or fruit juices for Ͼ5 to 6 years vitamin D, iron and calcium supplementation, and 1 multivitamin because of her limited preferences. Review of the nutritional con- daily. Her family was educated about dietary modification, and tent of her diet revealed essentially no dietary source of vitamin C her blood pressure was controlled on amlodipine and nadolol. for at least several years and limited amounts of vitamin D and Within 1 week of starting vitamin supplementation, her gingival iron (Table 1). Serum ascorbic acid level was 27 ␮mol/L (normal: bleeding and perifollicular purpura resolved, gingival swelling 11–85 ␮mol/L), but the sample was taken after several weeks of was markedly improved (Fig 3), and she no longer required consumption of hospital meals and is therefore not reflective of analgesia. There was significant improvement in the soft-tissue total body stores. Nutritional laboratory study results showed low swelling of the radii and knees and almost full range of motion of levels of serum ferritin (16 ␮g/L; normal: 22–400 ␮g/L), iron (0.6 her knees. Weight-bearing exercises were gradually introduced ␮mol/L; normal: 9–27 ␮mol/L), 25-OH-vitamin D (16 nmol/L; because of her osteopenia and compression fractures. Ten days normal: 25–90 nmol/L), and 1, 25-OH-vitamin D (32 pmol/L; after starting vitamin C supplementation, repeat radiographs of normal: 40–140 pmol/L). Serum B12 and red blood cell folate the lower extremities (Fig 4) showed fractures in the area of the left levels were normal. medial femoral metaphysis and a line of increased density sur- Investigations done for her hypertension included normal uri- rounding the epiphysis (Wimberger ring). Her hemoglobin in- nalyses, blood urea nitrogen, creatinine, Doppler renal ultrasound, creased to 125 g/L and her C-reactive protein normalized (6.6 diethylenetriaminepentaacetic acid renal scan, serum renin, and mg/L; normal: 0–8 mg/L) after 2 weeks of treatment. She was

2of5 AN ORANGEDownloaded A DAY KEEPS from www.aappublications.org/news THE DOCTOR AWAY by guest on September 25, 2021 Fig 3. Photograph demonstrating significant improvement in gingival swelling and resolution of gingival bleeding 10 days after treatment with vitamin C.

Fig 4. Anteroposterior radiograph of the left knee showing demi- Fig 5. Anteroposterior radiograph of the left knee performed af- neralization, metaphyseal lucent bands, and irregularity of the ter 6 months of vitamin C, showing healing in the region of the medial cortex of the distal femoral metaphysis in keeping with distal femoral metaphysis (arrow). fractures (arrow).

DISCUSSION ambulating with a walker as she had done previously by 6 weeks Unlike most animals, human beings lack the abil- and at her most recent follow-up after 6 months, her blood pres- ity to convert glucose to ascorbic acid (vitamin C) via sure was within normal limits for age while off all hypertensive medications. A radiograph of the left knee demonstrated resolu- gulonolactone oxidase, so that ascorbic acid in the tion of the metaphyseal spurs and lucencies, consistent with in- form of fresh fruits, vegetables, or vitamin supple- terval healing (Fig 5). ments is an essential nutrient in the human diet.1

Downloaded from www.aappublications.org/newshttp://www.pediatrics.org/cgi/content/full/108/3/ by guest on September 25, 2021 e55 3of5 Scurvy has been known to exist for more than 3 poor wound healing, edema, and alopecia.12 The role millennia with a description of a condition similar to of other concurrent nutritional deficiencies and med- it recorded by the ancient Egyptians in the Ebers ical conditions, however, contribute to clinical heter- papyrus.2 Not until 1753, however, was scurvy and ogeneity. Untreated scurvy can be fatal, with death its prevention by citrus fruits systematically de- ensuing from fulminant bacterial or tuberculous in- scribed by Sir James Lind, and ascorbic acid was first fection possibly related to poor wound healing,13 isolated in 1928.3 By the middle of the 20th century, cerebral hemorrhage, or hemopericardium.14 technological developments including food process- One aspect of this case that needs to be addressed ing and transportation combined to make scurvy a is whether this child’s presentation can be attributed rarely encountered disease. In a historical review by simply to a combination of rickets and iron defi- Lee4 of the medical records of the Yale-New Haven ciency. In fact, childhood scurvy was thought to be a Hospital from 1941 to 1971, there were 10 children complication of rickets until it was described as a with a diagnosis of scurvy, all occurring before 1949. separate entity in 1883.15 In contrast to experimen- Scurvy is still occasionally encountered, predomi- tally-induced scurvy, people with naturally acquired nantly among elderly, indigent persons who live disease often have generally deficient diets, which alone and prepare their own food, as well as in can contribute to the clinical presentation. However, alcoholics and food faddists. Scurvy is less common this child’s gingival disease and skin manifestations in the pediatric population, but case reports still cannot be explained by other nutritional deficiencies. appear.5,6 Groups at risk include infants who are fed Although a component of this child’s bone disease evaporated or boiled milk, in which ascorbic acid is may have been exacerbated by vitamin D deficiency, destroyed by heat and children with dietary restric- the radiographic findings were not suggestive of tions stemming from psychiatric or developmental rickets, and the normal levels of calcium, phosphate, disorders, such as the child described here. alkaline phosphatase, and parathyroid hormone do Ascorbic acid is a necessary cofactor in collagen not support vitamin D deficiency rickets as the pri- biosynthesis, and it is felt that the capillary fragility mary cause of the child’s bone disease. responsible for the clinical manifestations of scurvy An unusual aspect of this case was the presence of is attributable to the depletion of pericapillary colla- severe hypertension without an apparent secondary gen.7 Ascorbic acid has numerous physiologic prop- cause, despite a thorough investigation. Postural hy- erties, however, and other mechanisms are likely potension and syncope are reported to be common in involved. Signs of scurvy develop after 1 to 3 months untreated scurvy. Conversely, a preterminal event in of inadequate vitamin C intake, depending on exist- this condition may be frank hypertension progress- ing body stores.8 The earliest manifestations are der- ing to shock. Ascorbic acid is involved physiologi- matologic, with petechiae, ecchymoses, hyperkerato- cally in catecholamine biosynthesis and secretion,16 sis, and corkscrew hairs appearing at the onset of and there are animal and human data, which suggest naturally and experimentally-induced scurvy.9 As in a relationship between vitamin C status and blood our patient, the purpura is often localized to the pressure.17,18 It has been found that vitamin C levels perifollicular area. Gingival disease, characterized by in spontaneously hypertensive rats are lower than in swelling, ecchymoses, bleeding, and loosening of the controls, and that vitamin C supplementation de- teeth, usually occurs next in dentulous patients, also creased blood pressure in this rat model.19 Further- secondary to blood vessel instability. In contrast to more, epidemiologic studies have found a negative adults, bone disease is a frequent manifestation of correlation between vitamin C levels and blood pres- the condition in children, and, as in our patient, can sure, and several small-scale intervention trials have be debilitating. Pathologically, there is a defect of reported a decrease in blood pressure in borderline osteoid matrix formation and cartilage resorption hypertensives using vitamin C supplementation.20 leading to disordered bone structure and subsequent The resolution of this child’s hypertension along fractures around the growth plates.10 In addition, with her other signs of scurvy after treatment with subperiosteal hemorrhages can occur, leading to vitamin C is suggestive of a causal relationship be- bone pain. Anemia is another hallmark of scurvy and tween her hypertension and clear vitamin C defi- is multifactorial in nature. Iron deficiency anemia is ciency. common and may be secondary to a combination of As in the case illustrated here, other conditions bleeding, other dietary deficiencies, and decreased such as leukemia, musculoskeletal infections, and absorption. Ascorbic acid improves iron absorption vasculitides are often considered before the diagno- by reducing it to the more absorbable ferrous state,11 sis of scurvy is made because of the rarity of the and in our patient, who had absent bone marrow condition. A review of the medical records from 1980 iron stores, the anemia only improved after vitamin to the present at our institution, which is a tertiary C administration, despite 6 weeks of previous iron care pediatric facility with Ͼ50 000 emergency de- supplementation. Although nonspecific, an elevated partment visits per year, revealed 1 additional diag- erythrocyte sedimentation rate and C-reactive pro- nosis of scurvy. This patient was a teenaged female tein may be seen,5,10 which most likely reflects the with an eating disorder who had gingival bleeding inflammation involved in the bone and gingiva as and perifollicular purpura. The most important fac- was seen on biopsy in our patient. Other clinical tor in making the correct diagnosis is maintaining a signs of scurvy include skeletal muscle degeneration, high index of suspicion in the right clinical scenario. cardiac hypertrophy, diminished adrenal and bone The “four H’s” are a useful device for remembering marrow function, psychological changes, arthritis, many of the common presentations of scurvy: hem-

4of5 AN ORANGEDownloaded A DAY KEEPS from www.aappublications.org/news THE DOCTOR AWAY by guest on September 25, 2021 orrhagic signs, hyperkeratosis, hematologic abnor- Although rare, scurvy remains a condition that is malities, and hypochondriasis.1 In addition to clini- still encountered in the pediatric population, espe- cal signs, radiologic studies can be helpful. The most cially among certain groups with unusual eating common radiographic finding, however, is osteope- habits. A heightened awareness is needed to avoid nia, which is nonspecific, and the more specific signs unnecessary tests and procedures and to be able to for scurvy are less common and likely to be unfamil- implement treatment for a potentially fatal but easily iar to many radiologists because of the rarity of the curable disease. condition. Other radiographic findings include the preservation of the zones of calcification at the distal REFERENCES metaphyses with an adjacent lucency, referred to as 1. Levine M. 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Downloaded from www.aappublications.org/news by guest on September 25, 2021 An Orange a Day Keeps the Doctor Away: Scurvy in the Year 2000 Michael Weinstein, Paul Babyn and Stan Zlotkin Pediatrics 2001;108;e55 DOI: 10.1542/peds.108.3.e55

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